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Position Paper Diagnosis of Periodontal Diseases*

This position paper on the diagnosis of periodontal diseases was prepared by the Research, Science and Ther- apy Committee of the American Academy of . It is intended for the information of the dental profession and other interested parties. The purpose of the paper is to provide the reader with a general overview of the important issues related to the diagnosis of periodontal diseases. It is not intended as a com- prehensive review of the subject. J Periodontol 2003;74:1237-1247.

laque-induced periodontal diseases are mixed associated with connective tissue attachment loss also associated with relatively specific lead to the resorption of coronal portions of tooth- Pgroups of indigenous oral .1-6 Suscepti- supporting alveolar bone.16 bility to these diseases is highly variable and depends This simple separation of plaque-induced peri- on host responses to periodontal .7-11 odontal diseases into two categories is not as clear- Although bacteria cause plaque-induced inflammatory cut as it first appears. For example, if sites that have periodontal diseases, progression and clinical char- been successfully treated for periodontitis develop acteristics of these diseases are influenced by both some gingival inflammation at a later date, do those acquired and genetic factors that can modify sus- sites have recurrent periodontitis or super- ceptibility to .12-15 imposed on a reduced but stable ? There are currently no data to definitively answer TRADITIONAL APPROACH TO DIAGNOSIS this question. However, since not all sites with gin- Despite our increased understanding of the etiology givitis necessarily develop loss of attachment and and pathogenesis of periodontal infections, the diag- bone,17 it is reasonable to assume that gingivitis can nosis and classification of these diseases is still based occur on a reduced periodontium in which ongoing almost entirely on traditional clinical assessments.16,17 attachment loss is not occurring. A similar problem To arrive at a periodontal diagnosis, the must exists when the term “periodontitis” is assigned to rely upon such factors as: 1) presence or absence of sites with attachment loss and periodontal pockets clinical signs of inflammation (e.g., bleeding upon in which ongoing periodontal destruction is not probing); 2) probing depths; 3) extent and pattern of occurring. loss of clinical attachment and bone; 4) patient’s Demonstration of the progression of periodontitis medical and dental histories; and 5) presence or requires documentation of additional attachment loss absence of miscellaneous signs and symptoms, occurring between at least two time points. Since this including pain, ulceration, and amount of observable is not always possible, especially when a patient is plaque and .18-20 examined for the first time, most clinicians assign the Plaque-induced periodontal diseases have tradi- diagnosis of “periodontitis” to inflamed sites that also tionally been divided into two general categories based have loss of attachment and bone. This is a prudent on whether attachment loss has occurred: gingivitis practice since such sites may be either currently and periodontitis. Gingivitis is the presence of gingi- progressing or are at an increased risk for further val inflammation without loss of connective tissue periodontal destruction. Therefore, demonstration of attachment.16 Periodontitis can be defined as the pres- progressive attachment loss is not generally consid- ence of gingival inflammation at sites where there ered to be a requirement for using “periodontitis” as has been a pathological detachment of fibers a diagnostic label. from and the junctional has At the 1999 International Workshop for Classification migrated apically. In addition, inflammatory events of Periodontal Diseases and Conditions, a reclas- sification of the different forms of plaque-induced periodontal diseases was developed.21 This revised * This paper was developed under the direction of the Research, Science and Therapy Committee and approved by the Board of Trustees of the classification includes seven general types of plaque- American Academy of Periodontology in May 2003. induced periodontal diseases: 1) gingivitis, 2) chronic

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periodontitis, 3) , 4) periodon- pathogens in the subgingival flora might be useful in titis as a manifestation of systemic diseases, 5) necro- identifying a microbial target of periodontal therapy, tizing periodontal diseases, 6) abscesses of the but it does not provide information that is used in periodontium, and 7) periodontitis associated with determining a periodontal diagnosis. endodontic lesions.21 The major departures from the previous classification system are: 1) the term “chronic SCIENTIFIC EVALUATION OF DIAGNOSTIC periodontitis” has replaced “adult periodontitis” and TESTS 2) the term “aggressive periodontitis” has replaced Statistical validation of a potentially useful diagnostic “early-onset periodontitis.” In the new classification test routinely involves use of a two-by-two decision system, depending on a variety of circumstances, all matrix as shown in Figure 1. From such tables, the forms of periodontitis can progress rapidly or slowly validity of a diagnostic or prognostic test can be esti- and can be non-responsive to therapy. It was also mated.22 A diagnostic device or test is intended to acknowledged that gingivitis can develop on a reduced detect the presence of a specified disease. Data col- but stable periodontium.21 lection to evaluate a diagnostic test frequently employs The above classification should not be confused a cross-sectional sampling scheme, and the validity of with case types previously suggested by the American the test can be estimated by calculating its sensitivity Academy of Periodontology for purposes of third- and specificity. These can only be determined in a party insurance payments. The current case types cross-sectional study if the true disease status of the for periodontal diseases include: gingivitis (Case patient can be established from a single examination. Type I), mild periodontitis (Case Type II), moderate This is the case for the presence or absence of peri- periodontitis (Case Type III), advanced periodontitis odontitis. The sensitivity of a diagnostic test refers to (Case Type IV), and refractory periodontitis (Case the probability of the test being positive when the dis- Type V). ease is truly present. A perfect test would be able to detect the disease in all cases without registering a DIAGNOSTIC INFORMATION false negative. The sensitivity of such a perfect test Periodontal diagnoses are determined by analyzing would be 1.00. The specificity of a diagnostic test refers the information collected during a periodontal exam- to the probability of the test being negative when the ination. A decision is then made regarding the dis- disease is not present. A perfect test would be able to ease category that is most closely associated with correctly identify all instances in which the disease was the patient’s clinical status. The information routinely absent without registering a false positive. The speci- collected during a includes ficity of such a perfect test would be 1.00. However, in demographic data (e.g., age, gender, etc.), medical medicine and , perfect diagnostic tests do not history, history of previous and current periodontal exist. Therefore, a test’s sensitivity and specificity will problems, measurements (i.e., always be less than 1.00. It is reasonable to expect probing depths, , etc.), radio- that a clinically useful diagnostic test for periodontal dis- graphic findings, and miscellaneous clinical fea- eases should have high values for both sensitivity and tures or observations (e.g., gingival inflammation, specificity. There are, however, no preset upper and plaque/calculus, mobility, occlusal problems). In some lower limits of sensitivity and specificity values that situations, supplemental qualitative or quantitative determine if a diagnostic test is clinically useful. assessments of the gingival crevicular fluid (GCF) and Furthermore, since sensitivity and specificity values subgingival microflora are performed. In addition, a are calculated in diseased or healthy populations, genetic test for susceptibility to chronic periodonti- respectively, these values may be higher than calcula- tis has become commercially available.16 tions performed in a mixed population. In contrast, pre- It should be emphasized that, at the present time, dictive values are calculated in a mixed population of supplemental information on GCF components, the diseased and healthy patients. subgingival microflora, and genetic susceptibility are The positive predictive value of a test refers to the not commonly used by practitioners in arriving at a probability that the disease is present when the test is diagnosis since the diagnostic utility of this inform- positive. The negative predictive value refers to the ation has not been validated. Indeed, genetic testing probability that the disease is absent when the test is is primarily intended to assist in risk assessment and negative. However, predictive values are influenced by should not be considered a diagnostic test. In add- the prevalence of disease in a population. Thus, in a ition, testing for the presence of specific putative periodontal practice where there are many patients

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the risk of developing the disease at some point in the future. Calculations can be made by using the two-by-two contingency table (Fig. 2) to determine absolute risk, relative risk and odds ratios that are measures of the increased risk of developing the disease. Absolute risk refers to the probability that an individual will develop an adverse outcome over a specified time and can be calculated in prospective studies. Relative risk is the ratio of disease in an exposed group to the risk of disease in an unexposed group. It indicates the strength of the assessed relationship. The Figure 1. odds ratio measures the odds of having the Decision matrix for diagnostic and prognostic tests. exposure (risk factor) if the disease is present, divided by the odds of having the exposure if the disease is absent. It is usually calculated in retrospective studies and also indicates the strength of the association. It is important to note that relative risk and odds ratios refer to the strength of a relationship and cannot be used to predict what will occur. For example, if a test that is designed to identify high-risk sites for developing additional bone loss has an odds ratio of 15, it means that sites with a positive test are at a 15-fold higher risk of developing additional bone loss within a spec- ified time. For an in-depth analysis and dis- cussion of the statistical evaluation and interpretation of the validity of diagnostic tests, readers are referred to an excellent review of Figure 2. the subject.22 Contingency table for assessing risk. SUPPLEMENTAL DIAGNOSTIC TESTS Supplemental diagnostic tests can be used to with , a test may have a higher perform two basic tasks. The first is screening, i.e., predictive value than the same test in a general prac- to separate diseased from non-diseased patients. titioner’s office where there is a lower prevalence of The second is to detect sites or patients undergo- periodontitis. ing the progression of periodontitis. The second task In the current practice of periodontics, procedures is more demanding than the first. It is also of greater performed during the course of a routine periodon- importance since the clinician can easily separate tal examination are usually sufficient to identify sites healthy from periodontitis patients based on cus- that have undergone pathologic changes associated tomary clinical criteria. The clinical value of fully with periodontitis. Such examinations can detect sites validated diagnostic tests is considerable in that the with features of periodontitis such as the presence of results of such tests are potentially useful in identi- inflammation, periodontal pockets, local etiologic fac- fying the presence of therapeutic targets (i.e., puta- tors, and loss of clinical attachment and bone. How- tive pathogens), monitoring the response to therapy, ever, current periodontal examination procedures identifying sites at high risk for progression, and performed at a single visit cannot determine whether assisting the clinician in determining a patient- sites are currently undergoing additional attachment specific recall interval for periodontal maintenance loss. therapy. Several supplemental diagnostic tests are A prognostic device or test is intended to assess currently available and some are under develop-

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ment. Most of them are designed to provide inform- .19,72,93-104 Tissue breakdown products ation presumably associated with progressing peri- in GCF that have been suggested as possible mark- odontal lesions. ers for progressing periodontal lesions include gly- Supplemental diagnostic tests fall into four general cosaminoglycans105-110 and several bone-associated categories. They can be used to detect the presence proteins.59,67,111-116 of: 1) substances associated with putative pathogens; Chairside tests for asparate aminotransferase 2) host-derived enzymes; 3) tissue breakdown prod- (AST) and nonspecific neutral proteinases have been ucts; or 4) inflammatory mediators. developed. Dead and dying host cells release AST. Several strategies have been developed to detect Results from several longitudinal studies of chronic substances associated with putative periodontopatho- periodontitis patients in which increased clinical gens.19 They include DNA analyses,23-31 assessment attachment loss was used as the criterion for disease of antigenic profiles,32-41 and enzymatic activities of progression, suggest that the GCF content of AST certain members of the subgingival flora.42-52 The gen- might serve as a site-specific marker for ongoing eral aim of all of these approaches is to detect the periodontal destruction.57-62 Since AST is elevated presence of potentially in subgin- at sites with either gingivitis or nonprogressing peri- gival plaque samples. They have the advantage of not odontitis, it remains to be established if its levels in requiring the collection and preservation of viable bac- GCF can distinguish between sites that are breaking teria. Most of these tests can reliably identify sites that down and those that are not.19 harbor certain putative pathogens and thereby pro- The other GCF assay for host enzymes is a test for vide information about potential therapeutic targets. non-specific neutral proteinases. These lysosomal For example, if recently treated sites continue to har- enzymes are primarily derived from and bor high levels of pathogens, then it is reasonable to have been shown to be elevated in GCF from sites with conclude that additional therapy may be required. In advanced periodontitis.117-119 This enzyme-detection such instances, the tests could be used to monitor or system has not been longitudinally tested to deter- assess the endpoint or effectiveness of therapy with the mine if it can reliably detect sites at an increased risk ideal result being a negative test for the putative for progression. Neither the AST nor nonspecific pro- pathogens. One drawback of existing microbiologic teinase assays were originally marketed under the tests that do not culture the bacteria is that they are claim that they could detect progressing sites. They designed to detect only a limited number of pathogens. were simply sold as enzyme assays. It was left up to They cannot distinguish between virulent and avirulent the clinician to decide if the elevation of AST or neu- clones of putative pathogens. Another drawback is tral proteinases in GCF had any clinical relevance. their inability to provide any information about the Neither test is currently commercially available. sensitivities of the infecting bacteria. The Further development and clinical testing of certain only known way to determine antibiotic susceptibili- GCF-based diagnostic tests are warranted in order to ties of suspected pathogens is by cultural analysis and identify markers that are useful in identifying sites sensitivity testing of the subgingival flora.53-56 that are undergoing loss of periodontal attachment. An array of enzymes, tissue breakdown products, Such tests could be used to detect sites that require and inflammatory mediators are released from host additional treatment prior to, or during, the mainte- cells and tissues during the development and progres- nance phase of therapy. They also could be of value sion of periodontal infections. Some of these sub- in establishing optimal recall intervals for previously stances have been suggested as possible markers for treated patients. For example, patients with persis- the detection of progressing periodontal lesions. tently positive tests may require more frequent recall A number of studies have been conducted with the visits. In addition, patients who are in the most urgent general goal of devising chairside assays for mark- need of treatment might be more easily identified ers of disease progression in GCF.19 Host-derived through the use of such tests. enzymes that have received the most attention in In a research environment, function this regard are: aspartate aminotransferase,57-63 alka- assays and tests for -surface receptors can pro- line phosphatase,59,64-67 β-glucuronidase,59,68-72 elas- vide potentially useful diagnostic information. For tase,59,73-83 cathepsins,84-89 and dipeptidyl pepti- example, neutrophils from some patients with local- dase.84-85,90 Inflammatory mediators in GCF that ized aggressive periodontitis (LAgP) exhibit faulty might be associated with advancing periodontal chemotaxis and abnormal bactericidal activity.9 59,67,91-93 lesions include prostaglandin E2 and several Molecular markers of LAgP include an abnormally

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low number of chemoattractant receptors and an CAL is the distance from the cementoenamel junction abnormal amount of another cell-surface glycopro- to the base of the probeable crevice. Probing depth tein designated GP-110.120,121 On the other hand, measurements are clinically important since they patients with generalized aggressive periodontitis have provide a useful overall assessment of the depth of normal numbers of GP-110 receptors.120,121 It is prob- periodontal pockets which are the principal habitats able that tests of this type that are suitable for use of periodontal pathogens. In addition, PD measure- in clinical situations will eventually be developed. ments can be rapidly recorded and give a good However, at the present time, such tests are not assessment of the distribution of periodontal prob- available for widespread clinical application. lems within a given patient. They are an essential The only host-based test for susceptibility to component of a complete periodontal examination. periodontitis that is currently available to practitioners CAL assessments on the other hand are more is a genetic test for polymorphisms in the interleukin- difficult to accurately measure, but they give a better 1 (IL-1) gene cluster.15 The IL-1 gene cluster includes overall estimate of the amount of damage to the peri- IL-1A, IL-1B, and IL-1RN genes that code for IL-1α, odontium than do PD measurements. In prospective IL-1β, and the IL-1 receptor antagonist (IL-1ra) respec- studies, CAL measurements are the most valid method tively. Approximately 30% of Caucasians are positive for of assessing treatment outcomes.133 Multiple studies a composite genotype of IL-1A and IL-1B polymor- indicate that, in the hands of experienced practitioners, phisms consisting of allele 2 of both IL-1A + 4845 (or CAL measurements taken with conventional peri- the concordant -889) and IL-1B + 3954.15 People who odontal probes at different visits are repeatable to within carry this composite genotype may be at an increased ±1 mm more than 90% of the time.19,133 Under clini- risk of the following: bleeding upon probing,122 severe cal conditions, comparable repeatability values have ,15 tooth loss,123 and reduced sta- been obtained with computer-linked, controlled-force bility of gains of clinical attachment after guided tissue electronic periodontal probes.19,133 Electronic probes regeneration.124 Presumably this is due to hyper- have the advantage of controlling insertion forces and secretion of IL-1β in response to inflammation-inducing automatically recording clinical information into a com- stimuli.125 In contrast, other studies have noted that puter.19,133,134 In addition to controlled insertion force, the composite genotype cannot be used to identify electronic probes have a better resolution than standard patients that are predisposed to the following: tooth manual probes. This feature is important since it makes loss,126 periodontitis,127 attachment loss after ther- it theoretically feasible to detect smaller changes in apy,128 or increased secretion of IL-1β.129 Since there clinical attachment levels than are possible with man- is conflicting information in the literature, these con- ual probes.135 For example, in one study, untreated cepts need further validation. chronic periodontitis patients were examined over a It should also be noted that the prevalence of the 6-month period using a prototype of an automated IL-1 composite genotype is very low in some popu- probe which has an accuracy of 0.2 mm. It was found lations. For example, in people of Chinese heritage that if a threshold of 0.4 mm was used to indicate that only 2.3% are genotype-positive.130 In addition, the a change in attachment level had occurred, the preva- IL-1 genotype associated with increased risk of lence of sites that had progressed was 29% over the severe chronic periodontitis does not appear to be a 6-month period. If a large threshold (i.e., 2.4 mm), risk marker for aggressive forms of periodonti- comparable to that achievable with a manual probe tis.131,132 Therefore, in certain populations, the test was used, only 2% of the sites were determined to have is of little or no value in establishing the risk for experienced additional attachment loss.136 susceptibility to periodontitis. In conclusion, at pre- Manual (conventional) periodontal probes are highly sent, how best to use this genetic test in clinical satisfactory for the performance of routine periodon- practice has not been established. tal examinations. Comparable results are obtained when either manual or electronic probes are used.19 ADVANCES IN TRADITIONAL DIAGNOSTIC Some practitioners prefer electronic over conventional METHODS periodontal probes, especially because of the auto- In clinical practice, conventional periodontal probes matic data entry feature afforded by these devices. are widely used to obtain two important measure- The main drawback of electronic probes is their ten- ments: probing depth (PD) and clinical attachment dency to underestimate PD and CAL measurements loss (CAL). PD is defined as the distance from the in untreated patients.19 In such patients, the presence to the base of the probeable crevice. of subgingival calculus can interfere with probe inser-

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tion. To minimize this problem, reproducibility of clin- SUMMARY ical measurements taken with controlled-force probes At the present time, the diagnosis and classification of can be improved by using a “double-pass” method periodontal diseases are almost entirely based on (i.e., measuring each site twice).19,137,138 In treated traditional clinical assessments. Supplemental quanti- patients, this reproducibility problem is not as great. tative and qualitative assessments of the gingival Indeed, in treated patients, lower standard deviations crevicular fluid and subgingival microflora can poten- of replicate single-pass clinical measurements have tially provide useful information about the patient’s been obtained with controlled-force compared to con- periodontal disease. In certain situations, these supple- ventional probes.139,140 mental risk-assessment tests may be particularly In the past decade, many advances have been valuable in establishing the endpoint of therapy prior made in radiographic imaging methods for peri- to placing patients on a periodontal maintenance pro- odontal structures. Advanced direct digital (filmless) gram. Although the clinical utility of none of these tests radiographic and computed tomographic techniques has been validated, their further development is war- have been developed to the stage where they are ranted. A genetic test for susceptibility to periodon- already being used on a day-to-day basis by practi- titis has become commercially available. How best tioners.141 Intraoral radiographs, such as periapical to use this and future host-based tests in clinical prac- films and vertical or horizontal bitewings, provide a tice remains to be determined. Probing depth and considerable amount of information about the clinical attachment loss measurements obtained with periodontium that cannot be obtained by any other periodontal probes are practical and valid methods non-invasive means. The information supplied by for assessing periodontal status. Computer-linked, radiographs includes root length, root form, presence controlled-force electronic periodontal probes are or absence of periapical lesions, root proximity, and commercially available and are currently in use by estimates of remaining alveolar bone. Although valid some practitioners. Many of the logistical problems periodontal diagnoses cannot be made from radio- associated with subtraction radiography are being over- graphs alone, they are an essential component of a come and this powerful diagnostic tool may soon come complete periodontal examination.19 into widespread use. Future developments in this and Conventionally read radiographs routinely under- other imaging techniques are likely to have a profound estimate the amount of bone loss.19,142,143 In addition, effect on our approach to the diagnosis of periodontal sequentially taken radiographs, when examined by diseases. eye, are able to reveal changes in bone only after 30 to 50% of the bone mineral has been ACKNOWLEDGMENTS resorbed.135,141,144 Subtraction radiography, on the The primary author for this paper is Dr. Gary other hand, allows detection of changes in bone C. Armitage. Members of the Research, Science and density as low as 5%. Although subtraction radiogra- Therapy Committee include: Drs. Terry D. Rees, phy detects changes after they have occurred, it is Chair; Timothy Blieden; ; Vincent possible with this technique to detect very small J. Iacono; Joseph P. Fiorellini; Petros Damoulis; changes in alveolar bone that would go unnoticed with William V. Giannobile; Henry Greenwell; Angelo conventionally read films.135,136,141,145,146 Mariotti; Richard Nagy; Barry D. Wagenberg, Board Many of the logistical problems initially associated Liaison; Robert J. Genco, Consultant. with subtraction radiography are being overcome. Software programs have been developed to correct REFERENCES for subtle differences in contrast, projection geome- 1. Socransky SS, Haffajee AD. Microbial mechanisms in try, and other repeatability errors.141 Standardization the pathogenesis of destructive periodontal diseases: A of film positioning and angulation can be achieved by critical assessment. J Periodont Res 1991;26:195-212. 147 2. Socransky SS, Haffajee AD. The bacterial etiology of using a cephalostat or custom-made positioning destructive periodontal disease: Current concepts. 148 devices. Future development of subtraction radio- J Periodontol 1992;63:322-331. graphy techniques promises to have a profound 3. Moore WEC, Moore LVH. 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dinal study of prognostic factors in established peri- tory procedure to select an appropriate antibiotic for odontitis patients. J Clin Periodontol 1997;24:102-109. treatment of refractory periodontitis. J Periodontol 42. Eley BM, Cox SW. Correlation between gingivain/gin- 1986;57:325-327. gipain and bacterial didpeptidyl peptidase activity in 57. Chambers DA, Imrey PB, Cohen RL, Crawford JM, gingival crevicular fluid and periodontal attachment Alves MEAF, McSwiggin TA. A longitudinal study of loss in chronic periodontitis patients. A 2-year longi- aspartate aminotransferase in gingival crev- tudinal study. J Periodontol 1996;67:703-716. icular fluid. J Periodont Res 1991;26:65-74. 43. Amalfitano J, De Filippo AB, Bretz WA, Loesche WJ. 58. Magnusson I, Persson RG, Page RC, et al. 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Relationship rapid enzymatic assay in the field for the detection of between gingival crevicular fluid levels of aspartate infections associated with adult periodontitis. J Public aminotransferase and active tissue destruction in Health Dent 1993;53:235-240. treated chronic periodontitis patients. J Periodont Res 46. Drake CW, Hunt RJ, Beck JD, Zambon JJ. The distri- 1990;25:81-87. bution and interrelationship of Actinobacillus actino- 61. Persson GR, Page RC. Diagnostic characteristics of mycetemcomitans, , Prevotella crevicular fluid aspartate aminotransferase (AST) intermedia, and BANA scores among older adults. levels associated with periodontal disease activity. J Periodontol 1993;64:89-94. J Clin Periodontol 1992;19:43-48. 47. Hemmings KW, Griffiths GS, Bulman JS. Detection of 62. Persson GR, Alves MEAF, Chambers DA, et al. A mul- neutral protease (Periocheck) and BANA hydrolase ticenter clinical trial of PerioGard in distinguishing (Perioscan) compared with traditional clinical methods between diseased and healthy periodontal sites. J Clin of diagnosis and monitoring of chronic inflammatory Periodontol 1995;22:794-803. periodontal disease. J Clin Periodontol 1997;24:110-114. 63. Wong M-Y, Lu C-L, Liu C-M, Hou L-T, Chang W-K. 48. Loesche WJ, Lopatin DE, Giordano J, Alcoforado G, Relationship of the subgingival microbiota to a chair- Hujoel P. Comparison of the benzoyl-DL-arginine- side test for aspartate aminotransferase in gingival naphthylamide (BANA) test, DNA probes, and immuno- crevicular fluid. J Periodontol 1999;70:57-62. logical reagents for ability to detect anaerobic periodontal 64. Chapple ILC, Matthews JB, Thorpe GH, Glenwright HD, infections due to Porphyromonas gingivalis, Treponema Smith JM, Saxby MS. A new ultrasensitive chemilumi- denticola, and Bacteroides forsythus. J Clin Microbiol nescent assay for the site-specific quantification of alka- 1992;30:427-433. line phosphatase in gingival crevicular fluid. J Periodont 49. Loesche WJ, Kazor CE, Taylor GW. The optimization Res 1993;28:266-273. of the BANA test as a screening instrument for gingivitis 65. Chapple ILC, Glenwright HD, Matthews JB, Thorpe among subjects seeking dental treatment. J Clin GHG, Lumley PJ. Site-specific alkaline phosphatase Periodontol 1997;24:718-726. levels in gingival crevicular fluid in health and gingivi- 50. Smith AJ, Wade WG, Greenman J, Addy M. Analysis tis: Cross-sectional studies. J Clin Periodontol 1994;21: of cultivable Porphyromonas gingivalis with trypsin-like 409-414. protease enzyme activity and serum antibodies in 66. Chapple ILC, Socransky SS, Dibart S, Glenwright HD, chronic adult periodontitis. Oral Dis 1995;1:70-76. Matthews JB. Chemiluminescent assay of alkaline 51. Travis J, Pike R, Imamura T, Potempa J. Porphyromonas phosphatase in human gingival crevicular fluid: Inves- gingivalis proteinases as virulence factors in the devel- tigations with an experimental gingivitis model and opment of periodontitis. J Periodont Res 1997;32: studies on the source of the enzyme within crevicular 120-125. fluid. J Clin Periodontol 1996;23:587-594. 52. Watson M-R, Bretz WA, Loesche WJ. Presence of Tre- 67. Nakashima K, Roehrich N, Cimasoni G. Osteocalcin, ponema denticola and Porphyromonas gingivalis in prostaglandin E2 and alkaline phosphatase in gingival children correlated with periodontal disease of their crevicular fluid: Their relations to periodontal status. parents. J Dent Res 1994;73:1636-1640. J Clin Periodontol 1994;21:327-333. 53. Slots J, Rams TE, Listgarten MA. Yeasts, enteric rods and 68. Lamster IB, Oshrain RL, Harper DS, Celenti RS, Hovliaras pseudomonads in the subgingival flora of severe adult CA, Gordon JM. Enzyme activity in crevicular fluid for periodontitis. Oral Microbiol Immunol 1988;3:47-52. detection and prediction of clinical attachment loss in 54. Rams TE, Feik D, Slots J. Staphylococci in human peri- patients with chronic adult periodontitis: Six-month odontal diseases. Oral Microbiol Immunol 1990;5:29-32. results. J Periodontol 1988;59:516-523. 55. Walker CB, Gordon JM, Socransky SS. Antibiotic sus- 69. Lamster IB, Oshrain RL, Celenti RS, Fine JB, Grbic JT. ceptibility testing of subgingival plaque samples. J Clin Indicators of the acute inflammatory and humoral Periodontol 1983;10:422-432. immune responses in gingival crevicular fluid: Rela- 56. Telsey B, Oshrain HI, Ellison SA. A simplified labora- tionship to active periodontal disease. J Periodont Res

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1991;26:261-263. Res 1992;27:62-69. 70. Lamster IB, Holmes LG, Gross KBW, et al. The rela- 85. Eley BM, Cox SW. Cathepsin B/L-, elastase-, tryptase-, tionship of β-glucuronidase activity in crevicular fluid trypsin-, and dipeptidyl peptidase IV-like activities in to clinical parameters of periodontal disease. Findings gingival crevicular fluid: A comparison of levels before from a multicenter study. J Clin Periodontol 1994;21: and after periodontal surgery in chronic periodontitis 118-127. patients. J Periodontol 1992;63:412-417. 71. Lamster IB, Holmes LG, Gross KBW, et al. The rela- 86. Eley BM, Cox SW. The relationship between gingival tionship of β-glucuronidase activity in crevicular fluid crevicular fluid cathepsin B activity and periodontal to probing attachment loss in patients with adult attachment loss in chronic periodontitis patients: A periodontitis. Findings from a multicenter study. 2-year longitudinal study. J Periodont Res 1996;31: J Clin Periodontol 1995;22:36-44. 381-392. 72. Chung RM, Grbic JT, Lamster IB. Interleukin-8 and 87. Kunimatsu K, Mine N, Kato I, Hase T, Aoki Y, β-glucuronidase in gingival crevicular fluid. J Clin Yamamoto K. Possible functions of human neutrophil Periodontol 1997;24:146-152. serine proteinases, medullasin and cathepsin G, in 73. Palcanis KG, Larjava IK, Wells BR, et al. Elastase as periodontal tissue breakdown. J Periodont Res 1993; an indicator of periodontal disease progression. J Peri- 28:547-549. odontol 1992;63:237-242. 88. Kunimatsu K, Mine N, Muraoka Y, et al. Identification 74. Armitage GC, Jeffcoat MK, Chadwick DE, et al. and possible function of cathepsin G in gingival cre- Longitudinal evaluation of elastase as a marker for vicular fluid from chronic adult periodontitis patients the progression of periodontitis. J Periodontol 1994;65: and from experimental gingivitis subjects. J Periodont 120-128. Res 1995;30:51-57. 75. 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The use of Suomalainen K, Sorsa T. , gelatinase and crevicular fluid prostaglandin E2 levels as a predictor of elastase activities in sulcular fluid of osseointegrated periodontal attachment loss. J Periodont Res 1986; implants and natural teeth. J Clin Periodontol 1994; 21:101-112. 21:301-307. 92. Nelson SL, Hynd BA, Pickrum HM. Automated enzyme 78. Alavi AL, Palmer RM, Odell EW, Coward PY, Wilson RF. immunoassay to measure prostaglandin E2 in gingival Elastase in gingival crevicular fluid from smokers and crevicular fluid. J Periodont Res 1992;27: 143-148. non-smokers with chronic inflammatory periodontal 93. Alexander DCC, Martin JC, King PJ, Powell JR, disease. Oral Dis 1995;1:110-114. Caves J, Cohen ME. Interleukin-1 beta, prostaglandin 79. Jin LJ, Söder P-Ö, Åsman B, Bergström K. Granulocyte E2, and subclasses in gingival elastase in gingival crevicular fluid: Improved monitor- crevicular fluid in patients undergoing periodontal ther- ing of the site-specific response to treatment in patients apy. J Periodontol 1996;67:755-762. with destructive periodontitis. J Clin Periodontol 1995; 94. Geivelis M, Turner DW, Pederson ED, Lamberts BL. 22:240-246. Measurements of interleukin-6 in gingival crevicular 80. Meyer J, Guessous F, Huynh C, et al. Active and α-1 fluid from adults with destructive periodontal disease. proteinase inhibitor complexed leukocyte elastase levels J Periodontol 1993;64:980-983. in crevicular fluid from patients with periodontal dis- 95. Payne JB, Reinhardt RA, Masada MP, DuBois LM, eases. J Periodontol 1997;68:256-261. Allison AC. Gingival crevicular fluid IL-8: Correlation 81. Murray MC, Mooney J, Kinane DF. The relationship with local IL-1β levels and patient estrogen status. between elastase and lactoferrin in healthy, gingivitis J Periodont Res 1993;28:451-453. and periodontitis sites. Oral Dis 1995;1:106-109. 96. Reinhardt RA, Masada MP, Kaldahl WB, et al. Gingival 82. Smith QT, Harriman L, Au GS, et al. Neutrophil elastase fluid IL-1 and IL-6 levels in refractory periodontitis. in crevicular fluid: Comparison of a middle-aged J Clin Periodontol 1993;20:225-231. general population with healthy and periodontitis 97. Reinhardt RA, Masada MP, Johnson GK, DuBois LM, groups. J Clin Periodontol 1995;22:935-941. Seymour GJ, Allison AC. IL-1 in gingival crevic- 83. Uitto VJ, Nieminen A, Coil J, Hurttia H, Larjava H. Oral ular fluid following closed root planing and pap- fluid elastase as an indicator of periodontal health. illary flap . J Clin Periodontol 1993;20: J Clin Periodontol 1996;23:30-37. 514-519. 84. Eley BM, Cox SW. Cathepsin B/L-, elastase-, tryptase-, 98. Preiss DS, Meyle J. Interleukin-1β concentration of trypsin-, and dipeptidyl peptidase IV-like activities in gin- gingival crevicular fluid. J Periodontol 1994;65:423- gival crevicular fluid: Correlation with clinical parameters 428. in untreated chronic periodontitis patients. J Periodont 99. Reinhardt RA, Masada MP, Payne JB, Allison AC,

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DuBois LM. Gingival fluid IL-1β and IL-6 levels in 64:865-869. menopause. J Clin Periodontol 1994;21:22-25. 116. Giannobile WV, Lynch SE, Denmark RG, Paquette DW, 100. Hou L-T, Liu C-M, Rossomando EF. Crevicular Fiorellini JP, Williams RC. Crevicular fluid osteocalcin interleukin-1β in moderate and severe periodontitis and pyridinoline cross-linked carboxyterminal telopep- patients and the effect of phase I periodontal treat- tide of type I collagen (ICTP) as markers of rapid bone ment. J Clin Periodontol 1995;22:162-167. turnover in periodontitis. A pilot study in beagle dogs. 101. Guillot JL, Pollock SM, Johnson RB. Gingival J Clin Periodontol 1995;22:903-910. interleukin-6 concentration following phase I therapy. 117. Bowers JE, Zahradnik RT. Evaluation of a chairside J Periodontol 1995;66:667-672. gingival protease test for use in periodontal diagno- 102. Tsai C-C, Ho Y-P, Chen C-C. Levels of interleukin-1β sis. J Clin Dent 1989;1:106-109. and interleukin-8 in gingival crevicular fluids in adult 118. Bowers JE, Hawley CE, Romberg E. A clinical test for periodontitis. J Periodontol 1995;66:852-859. proteolytic enzymes in gingival crevicular fluid: Com- 103. Lee H-J, Kang I-K, Chung C-P, Choi S-M. The sub- parison with periodontal probing depth and bleeding gingival microflora and gingival crevicular fluid on probing. Int J Periodontics Restorative Dent 1991; cytokines in refractory periodontitis. J Clin Periodon- 11:411-422. tol 1995;22:885-890. 119. Bader HI, Boyd RL. Long-term monitoring of adult 104. Mathur A, Michalowicz B, Castillo M, Aeppli D. periodontitis patients in supportive periodontal ther- Interleukin-1 alpha, interleukin-8 and interferon-alpha apy: Correlation of gingival crevicular fluid proteases levels in gingival crevicular fluid. J Periodont Res with probing attachment loss. J Clin Periodontol 1999; 1996;31:489-495. 26:99-105. 105. Giannobile WV, Riviere GR, Gorski JP, Tira DE, 120. Van Dyke TE, Wilson-Burrows C, Offenbacher S, Cobb CM. Glycosaminoglycans and periodontal dis- Henson P. Association of an abnormality of neutrophil ease: Analysis of GCF by safranin O. J Periodontol chemotaxis in human periodontal disease with a cell 1993;64:186-190. surface protein. Infect Immun 1987;55:2262-2267. 106. Samuels RHA, Pender N, Last KS. The effects of 121. Van Dyke TE, Warbington M, Gardner M, Offenbacher S. orthodontic tooth movement on the glycosaminoglycan Neutrophil surface protein markers as indicators component of gingival crevicular fluid. J Clin Periodontol of defective chemotaxis in LJP. J Periodontol 1990;61: 1993;20:371-377. 180-184. 107. Embery G, Waddington R. Gingival crevicular fluid: 122. Lang NP, Tonetti MS, Suter J, et al. Effect of Biomarkers of periodontal tissue activity. 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Scand J Dent Res treated periodontal patients over 10 years. J Periodontol 1992;100:107-110. 2001;72:767-773. 113. Talonpoika JT, Hämäläinen MM. Collagen I car- 127. Papapanou PN, Neiderud AM, Sandros J, Dahlen G. boxyterminal propeptide in human gingival crevicular Interleukin-1 gene polymorphism and periodontal fluid before and after periodontal treatment. Scand J status. A case-control study. J Clin Periodontol 2001; Dent Res 1993;101:154-158. 28:389-396. 114. Talonpoika JT, Hämäläinen MM. Type I collagen 128. Ehmke B, Kress W, Karch H, Grimm T, Klaiber B, carboxyterminal telopeptide in human gingival crevicular Flemmig TF. Interleukin-1 haplotype and periodontal fluid in different clinical conditions and after periodon- disease progression following therapy. J Clin Peri- tal treatment. J Clin Periodontol 1994;21:320-326. odontol 1999;26:810-813. 115. Kunimatsu K, Mataki S, Tanaka H, et al. A cross- 129. Mark LL, Haffajee AD, Socransky SS, et al. 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2000;35:1172-1177. 146. Jeffcoat MK, Reddy MS. Digital subtraction radiog- 130. Armitage GC, Wu Y, Wang H-Y, Sorrell J, di Giovine FS, raphy for longitudinal assessment of peri-implant Duff GS. Low prevalence of a periodontitis-associated bone change: Method and validation. Adv Dent Res interleukin-1 composite genotype in individuals of Chi- 1993;7:196-201. nese heritage. J Periodontol 2000;71:164-171. 147. Jeffcoat MK, Reddy MS, Webber RL, Williams RC, 131. Diehl SR, Wang YF, Brooks CN, et al. Linkage dis- Ruttimann UE. Extraoral control of geometry for dig- equilibrium of interleukin-1 genetic polymorphisms ital subtraction radiography. J Periodont Res 1987; with early-onset periodontitis. J Periodontol 1999;70: 22:396-402. 418-430. 148. Hausmann E, Christersson L, Dunford R, Wikesjö U, 132. Walker SJ, Van Dyke TE, Rich S, Kornman KS, di Phyo J, Genco RJ. Usefulness of subtraction radi- Giovine FS, Hart TC. Genetic polymorphisms of the ography in the evaluation of periodontal therapy. IL-1α and IL-1β genes in African-American LJP J Periodontol 1985;56(Suppl.):4-7. patients and an African-American control population. 149. Jeffcoat MK. Radiographic methods for the detection J Periodontol 2000;71:723-728. of progressive alveolar bone loss. J Periodontol 1992; 133. Armitage GC. Manual periodontal probing in supportive 63:367-372. periodontal treatment. Periodontol 2000 1996;12:33-39. 150. Hausmann E, Allen K, Norderyd J, Ren W, Shibly O, 134. Magnusson I. Computerized periodontal probing. Machtei E. Studies on the relationship between changes Periodontol 2000 1996;12:40-43. in radiographic bone height and probing attachment. 135. Jeffcoat MK, Reddy MS. A comparison of probing and J Clin Periodontol 1994;21:128-132. radiographic methods for detection of periodontal dis- ease progression. Curr Opin Dent 1991;1:45-51. Individual copies of this paper may be obtained on the 136. Jeffcoat MK, Reddy MS. Progression of probing Academy’s Web site at http://www.perio.org. Members of the attachment loss in adult periodontitis. J Periodontol American Academy of Periodontology have permission of 1991;62:185-189. the Academy, as copyright holder, to reproduce up to 137. Osborn J, Stoltenberg J, Huso B, Aeppli D, Pihlstrom B. 150 copies of this document for not-for-profit, educational Comparison of measurement variability using a stan- purposes only. For information on reproduction of the docu- dard and constant force periodontal probe. J Periodontol ment for any other use or distribution, please contact Rita 1990;61:497-503. Shafer at the Academy Central Office; voice: 312/573-3221; 138. Osborn JB, Stoltenberg JL, Huso BA, Aeppli DM, fax: 312/573-3225; or e-mail: [email protected]. Pihlstrom BL. Comparison of measurement variability in subjects with moderate periodontitis using a con- ventional and constant force periodontal probe. J Peri- odontol 1992;63:283-289. 139. Yang MCK, Marks RG, Magnusson I, Clouser B, Clark WB. Reproducibility of an electronic probe in relative attachment level measurements. J Clin Periodontol 1992;19:541-548. 140. Rams TE, Slots J. Comparison of two pressure-sensitive periodontal probes and a manual periodontal probe in shallow and deep pockets. Int J Periodontics Restora- tive Dent 1993;13:521-529. 141. Jeffcoat MK, Wang I-C, Reddy MS. Radiographic diag- nosis in periodontics. Periodontol 2000 1995;7:54-68. 142. Albandar JM. Validity and reliability of alveolar bone level measurements made on dry skulls. J Clin Peri- odontol 1989;16:575-579. 143. Åkesson L, Håkansson J, Rohlin M. Comparison of panoramic and intraoral radiography and pocket prob- ing for the measurement of the marginal bone level. J Clin Periodontol 1992;19:326-332. 144. Ortman LF, McHenry K, Hausmann E. Relation- ship between alveolar bone measured by 125I absorp- tiometry with analysis of standardized radiographs. 2. Bjorn technique. J Periodontol 1982;53:311-314. 145. Reddy M. Radiographic methods in the evaluation of periodontal therapy. J Periodontol 1992;63:1078- 1084.

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